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A Gene-Tree Test of the Traditional Taxonomy of American Deer

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A Gene-Tree Test of the Traditional Taxonomy of American Deer A peer-reviewed open-access journal ZooKeys 697: 87–131 (2017)A gene-tree test of the traditional taxonomy of American deer... 87 doi: 10.3897/zookeys.697.15124 RESEARCH ARTICLE http://zookeys.pensoft.net Launched to accelerate biodiversity research A gene-tree test of the traditional taxonomy of American deer: the importance of voucher specimens, geographic data, and dense sampling Eliécer E. Gutiérrez1,2,3,4, Kristofer M. Helgen5, Molly M. McDonough3,4, Franziska Bauer6, Melissa T. R. Hawkins3,4, Luis A. Escobedo-Morales7, Bruce D. Patterson8, Jesús E. Maldonado4,9 1 PPG Biodiversidade Animal, Centro de Ciências Naturais e Exatas, Av. Roraima n. 1000, Prédio 17, sala 1140- D, Universidade Federal de Santa Maria, Santa Maria, RS 97105-900, Brazil 2 Departamento de Zoologia, Universidade de Brasília, 70910-900 Brasília, DF, Brazil 3 Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington DC, USA 4 Center for Conservation Genomics, National Zoological Park, Smithsonian Institution, Washington DC, USA 5 School of Biological Sciences and Environment Institute, University of Adelaide, Adelaide, South Australia 5005, Australia 6 Museum of Zoology, Senckenberg Natural History Collections, Dresden, Germany 7 Instituto de Biología, Universidad Nacional Autónoma de México, circuito exterior s/n, Ciudad Universitaria, Coyoacán, CP04510, Mexico City, Mexico 8 Integrative Research Center, Field Museum of Natural History, Chicago, IL60605, USA 9 Environmental Science & Policy, George Mason University, 4400 University Dr., Fairfax, VA 22030, USA Corresponding author: Eliécer E. Gutiérrez ([email protected]) Academic editor: Yasen Mutafchiev | Received 17 July 2017 | Accepted 30 August 2017 | Published 14 September 2017 http://zoobank.org/9A9DB3EF-BB88-48AD-B966-06CD5ADBB25E Citation: Gutiérrez EE, Helgen KM, McDonough MM, Bauer F, Hawkins MTR, Escobedo-Morales LA, Patterson BD, Maldonado JE (2017) A gene-tree test of the traditional taxonomy of American deer: the importance of voucher specimens, geographic data, and dense sampling. ZooKeys 697: 87–131. https://doi.org/10.3897/zookeys.697.15124 Abstract The taxonomy of American deer has been established almost entirely on the basis of morphological data and without the use of explicit phylogenetic methods; hence, phylogenetic analyses including data for all of the currently recognized species, even if based on a single gene, might improve current understand- ing of their taxonomy. We tested the monophyly of the morphology-defined genera and species of New World deer (Odocoileini) with phylogenetic analyses of mitochondrial DNA sequences. This is the first such test conducted using extensive geographic and taxonomic sampling. Our results do not support the Copyright Eliécer E. Gutiérrez et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 88 Eliécer E. Gutiérrez et al. / ZooKeys 697: 87–131 (2017) monophyly of Mazama, Odocoileus, Pudu, M. americana, M. nemorivaga, Od. hemionus, and Od. virgin- ianus. Mazama contains species that belong to other genera. We found a novel sister-taxon relationship between “Mazama” pandora and a clade formed by Od. hemionus columbianus and Od. h. sitkensis, and transfer pandora to Odocoileus. The clade formed by Od. h. columbianus and Od. h. sitkensis may represent a valid species, whereas the remaining subspecies of Od. hemionus appear closer to Od. virginianus. Pudu (Pudu) puda was not found sister to Pudu (Pudella) mephistophiles. If confirmed, this result will prompt the recognition of the monotypic Pudella as a distinct genus. We provide evidence for the existence of an undescribed species now confused with Mazama americana, and identify other instances of cryptic, taxonomically unrecognized species-level diversity among populations here regarded as Mazama temama, “Mazama” nemorivaga, and Hippocamelus antisensis. Noteworthy records that substantially extend the known distributions of M. temama and “M.” gouazoubira are provided, and we unveil a surprising ambi- guity regarding the distribution of “M.” nemorivaga, as it is described in the literature. The study of deer of the tribe Odocoileini has been hampered by the paucity of information regarding voucher specimens and the provenance of sequences deposited in GenBank. We pinpoint priorities for future systematic research on the tribe Odocoileini. Keywords Deer, Cervidae, Neotropics, Americas, Taxonomy, Odocoileus, Mazama, Pudu, Hippocamelus, phylogenetics, mDNA, CYTB Introduction The tribe Odocoileini (Cervidae: Capreolinae) represents a monophyletic group en- compassing all modern deer native to the New World (Americas) with the exception of the Holarctic taxa Alces alces (Alceini), Cervus canadensis (Cervini), and Rangifer taran- dus (Rangiferini) (Price et al. 2005, Gilbert et al. 2006, Hughes et al. 2006, Agnarsson and May-Collado 2008, Decker et al. 2009, Hassanin et al. 2012, Heckeberg et al. 2016)—see Heckeberg et al. (2016) for current suprageneric taxonomy. Living Odo- coileini deer have been traditionally classified in six genera Blastocerus( , Hippocamelus, Mazama, Odocoileus, Ozotoceros, and Pudu) and 16 species (Merino and Rossi 2010, Mattioli 2011; see also Gutiérrez et al. 2015), but alternative taxonomic propositions have suggested that the alpha-level diversity of the tribe might be higher (Molina and Molinari 1999, Molinari 2007, Groves and Grubb 2011). Some authors have also in- cluded Rangifer as a member of Odocoileini (e.g., Groves and Grubb 2011). The native distribution of Odocoileini ranges from northern North America (Alas- ka, Canada) to southern South America (Patagonia), including some islands of the Caribbean Sea and the Atlantic and Pacific oceans. Collectively, members of the tribe occupy a wide variety of habitats, including desert scrub, savannas, swamps, lowland rain forests, humid-montane forests, páramo, and alpine tundra at elevations from sea level to about 4800 meters (Allen 1915, Hershkovitz 1982, Baker 1984, Méndez 1984, Brokx 1984, Medellín et al. 1998, González et al. 2002, Cronin et al. 2006, Meier and Merino 2007, Molinari 2007, Rumiz et al. 2007, Latch et al. 2009, Miran- da et al. 2009, Piovezan et al. 2010, Groves and Grubb 2011, Mendes-Oliveira et al. A gene-tree test of the traditional taxonomy of American deer... 89 2011, Barrio 2013, Gutiérrez et al. 2015). By virtue of this wide ecogeographic range, Odocoileini is of great biogeographic interest. Despite being heavily hunted animals in the Western Hemisphere and also of great public health interest (Bennett and Robinson 2000, Hurtado-Gonzales and Bodmer 2004, Angers et al. 2006, Campbell and VerCauteren 2011, Martinsen et al. 2016, Ue- hlinger et al. 2016), relatively little progress has been achieved in recent decades with regard to the systematics of Odocoileini deer. To date, only the genera Mazama (Allen 1915) and Pudu (Hershkovitz 1982) have been subjects of specimen-based revisionary taxonomic work, but these studies did not employ explicit phylogenetic methods. In general, the scientific community has largely followed the taxonomic arrangements recognized by 20th century authorities, predominantly E. R. Hall for North America (Hall 1981) and A. Cabrera for South America (Cabrera 1961). The uncritical accept- ance of these taxonomic arrangements for decades is indefensible because the criteria, data, and methods used to construct them are largely unknown, unclear, or even in- correct (see example pointed out by Molinari [2007, p. 31]). Several recent taxonomic studies have demonstrated that the traditional taxonomy of Odocoileini deer needs to be revisited. For instance, morphometric analyses and differences in the frequency of qualitative skeletal traits in Odocoileus virginianus of northern South America and North America led Molina and Molinari (1999) to propose that populations from North and South America are not conspecific. These authors also demonstrated a -re markable degree of morphological variability among Venezuelan populations of Od. virginianus, whose taxonomy remains disputed (Moscarella et al. 2003, 2007, Molinari 2007). Another example comes from phylogenetic analyses of molecular data dem- onstrating that the genus Mazama, as traditionally understood (Allen 1915, Cabrera 1961), is polyphyletic (Gilbert et al. 2006, Duarte et al. 2008, Hassanin et al. 2012, Escobedo-Morales et al. 2016, Heckeberg et al. 2016). Unfortunately, phylogenetic studies of Odocoileini published to date have been based on limited taxonomic and/or geographic sampling—i.e., lacking taxa or using exemplars for widely distributed and highly variable taxa (e.g., species of Odocoileus). Nevertheless, these and other taxo- nomic studies, some based on karyology (e.g., Jorge and Benirschke 1977, Duarte and Jorge 2003, Cursino et al. 2014), have documented the need to revise the systematics of Odocoileini deer. Biologically meaningful species-level taxonomies are essential for study design in evolutionary biology, and inadequate species-level classifications, such as uncriti- cally lumping or splitting taxa in absence of appropriate evidence, can detrimentally impact species conservation (George and Mayden 2005, Gutiérrez and Helgen 2013, Heller et al. 2013, Kaiser et al. 2013, Zachos et al. 2013, Voigt et al. 2015, Gippoliti et al. 2017). Accordingly, our long-term goal
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